HSP27, 70 and 90, anti-apoptotic proteins, in clinical cancer therapy (review)

International Journal of Oncology

Volumn 45, Issue 1, 2014, Pages 18-30

  Wang, Xiaoxia ^a   Chen, Meijuan ^a   Zhou, Jing ^a   Zhang, Xu ^a  

^a NANJING UNIVERSITY OF CHINESE MEDICINE   (China)

Author keywords

Apoptosis; Cancer; Heat shock proteins 27, 70 and 90

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ANTINEOPLASTIC AGENT; APTAMER; HEAT SHOCK PROTEIN 27; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 70 INHIBITOR; HEAT SHOCK PROTEIN 90; HEAT SHOCK PROTEIN 90 INHIBITOR; HEAT SHOCK TRANSCRIPTION FACTOR 1; UNCLASSIFIED DRUG; HEAT SHOCK PROTEIN;

AMINO TERMINAL SEQUENCE; APOPTOSIS; CANCER THERAPY; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN STRUCTURE; PROTEIN TARGETING; REVIEW; ANIMAL; ANTAGONISTS AND INHIBITORS; CHEMISTRY; METABOLISM; NEOPLASMS; PATHOLOGY;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; HEAT-SHOCK PROTEINS; HSP27 HEAT-SHOCK PROTEINS; HSP70 HEAT-SHOCK PROTEINS; HSP90 HEAT-SHOCK PROTEINS; HUMANS; NEOPLASMS;

EID: 84902581942     PISSN: 10196439     EISSN: 17912423     Source Type: Journal    
DOI: 10.3892/ijo.2014.2399     Document Type: Review

References (124)

1. Young JC, Agashe VR, Siegers K and Hartl FU: Pathways of chaperone-mediated protein folding in the cytosol. Nat Rev Mol Cell Biol 5: 781-791, 2004.
2. Lindquist S and Craig EA: The heat-shock proteins. Annu Rev Genet 22: 631-77, 1998.
3. Lebret T, Watson RW and Fitzpatrick JM: Heat shock proteins: their role in urological tumours. J Urolog 169: 338-346, 2003.
4. Khalil AA, Kabapy NF, Deraz SF and Smith C: Heat shock proteins in oncology: diagnostic biomarkers or therapeutic targets? Biochim Biophys Acta 1816: 89-104, 2011.
5. Jego G, Hazoumé A, Seigneuric R and Garrido C: Targeting heat shock proteins in cancer. Cancer Lett 332: 275-285, 2013.
6. Xia Y, Rocchi P, Iovanna JL and Peng L: Targeting heat shock response pathways to treat pancreatic cancer. Drug Discov Today 17: 35-43, 2012.
7. Garrido C, Brunet M, Didelot C, Zermati Y, Schmitt E and Kroemer G: Heat shock proteins 27 and 70: anti-apoptotic proteins with tumorigenic properties. Cell Cycle 5: 2592-2601, 2006.
8. Joly AL, Wettstein G, Mignot G, Ghiringhelli F and Garrido C: Dual role of heat-shock proteins as regulator of apoptosis and innate immunity. J Innate Immun 2: 238-247, 2010.
9. Wei MC, Zong WX, Cheng EH, Lindsten T, Panoutsakopoulou V, Ross AJ, Roth KA, MacGregor GR, Thompson CB and Korsmeyer SJ: Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death. Science 292: 727-30, 2001.
10. Zong WX, Lindsten T, Ross AJ, MacGregor GR and Thompson CB: BH3-only proteins that bind pro-survival Bcl-2 family members fail to induce apoptosis in the absence of Bax and Bak. Genes Dev 15: 1481-1486, 2001.
11. Garrido C, Galluzzi L, Brunet M, Puig PE, Didelot C and Kroemer G: Mechanisms of cytochrome c release from mitochondria. Cell Death Differ 13: 1423-1433, 2006.
12. Li P, Nijhawan D, Budihardjo I, Srinivasula SM, Ahmad M, Alnemri ES and Wang X: Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 91: 479-489, 1997.
13. Joza N, Susin SA, Daugas E, Stanford WL, Cho SK, Li CY, Sasaki T, Elia AJ, Cheng HY, Ravagnan L, Ferri KF, Zamzami N, Wakeham A, Hakem R, Yoshida H, Kong YY, Mak TW, Zuniga-Pflucker JC, Kroemer G and Penninger JM: Essential role of the mitochondrial apoptosis-inducing factor in programmed cell death. Nature 410: 549-554, 2001.
14. Du C, Fang M, Li Y, Li L and Wang X: Smac, a mitochondrial protein that promotes cytochrome c-dependent caspase activation by eliminating IAP inhibition. Cell 102: 33-42, 2000.
15. Luo X, Budihardjo I, Zou H, Slaughter C and Wang X: Bid, a Bcl2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors. Cell 94: 481-490, 1998.
16. Shamovsky I and Nudler E: New insights into the mechanism of heat shock response activation. Cell Mol Life Sci 65: 855-861, 2008.
17. Akerfelt M, Morimoto RI and Sistonen L: Heat shock factors: integrators of cell stress, developmentand lifespan. Nat Rev Mol Cell Biol 11: 545-555, 2010.
18. Green M, Schuetz TJ, Sullivan EK and Kingston RE: A heat-shock responsive domain of human HSF1 that regulates transcription activation domain function. Mol Cell Biol 15: 3354-3362, 1995.
19. Sistonen L, Sarge KD and Morimoto RI: Human heat shock factors 1and 2 are differentially activated and can synergistically induce hsp70 gene transcription. Mol Cell Biol 14: 2087-2099, 1994.
20. Nakai A, Tanabe M, Kawazoe Y, Inazawa J, Morimoto RI and Nagata K: HSF4, a new member of the human heat shock factor family which lacks properties of a transcriptional activator. Mol Cell Biol 17: 469-481, 1997.
21. Akerfelt M, Trouillet D, Mezger V and Sistonen L: Heat shock factors at a cross road between stress and development. Ann NY Acad Sci 1113: 15-27, 2007.
22. Abane R and Mezger V: Roles of heat shock factors in gametogenesis and development. FEBS J 277: 4150-4172, 2010.
23. Whitesell L and Lindquist S: Inhibiting the transcription factor HSF1 as an anticancer strategy. Expert Opin Ther Targets 13: 469-478, 2009.
24. Westerheide SD, Kawahara TL, Orton K and Morimoto RI: Triptolide, an inhibitor of the human heat shock response that enhances stress-induced cell death. J Biol Chem 281: 9616-9622, 2006.
25. SugiyamaY, Suzuki A, Kishikawa M, Akutsu R, Hirose T and Waye MM: Muscle develops a specific form of small heat shock protein complex composed of MKBP/HSPB2 and HSPB3 during myogenic differentiation. J Biol Chem 275: 1095-1104, 2000.
26. KostenkoS and Moens U: Heat shock protein 27 phosphorylation: kinases, phosphatases, functions and pathology. Cell Mol Life Sci 66: 3289-3307, 2009.
27. Shin KD, Lee MY, Shin DS, Lee S, Son KH, Koh S, Paik YK, Kwon BM and Han DC: Blocking tumor cell migration and invasion with biphenyl isoxazole derivative KRIBB3, a synthetic molecule that inhibits Hsp27 phosphorylation. J Biol Chem 280: 41439-41448, 2005.
28. Gobbo J, Gaucher-Di-Stasio C, Weidmann S, Guzzo J and Garrido C: Quantification of HSP27 and HSP70 molecular chaperone activities. Methods Mol Biol 787: 137-143, 2011.
29. Bruey JM, Paul C, Fromentin A, Hilpert S, Arrigo AP, Solary E and Garrido C: Differential regulation of HSP27 oligomerization in tumor cells grown in vitro and in vivo. Oncogene 19: 4855-4863, 2000.
30. Shashidharamurthy R, Koteiche HA, Dong J and McHaourab HS: Mechanism of chaperone function in small heat shock proteins: Dissociation of the HSP27 oligomer is required for recognition and binding of destabilized T4 lysozyme. J Biol Chem 280: 5281-5289, 2005
31. Charette SJ, Lavoie JN, Lambert H and Landry J: Inhibition of Daxx-mediated apoptosis by heat shock protein 27. Mol Cell Biol 20: 7602-7612, 2000.
32. Akbar MT, Lundberg AM, Liu K, Vidyadaran S, Wells KE, Dolatshad H, Wynn S, Wells DJ, Latchman DS and de Belleroche J: The neuroprotective effects of heat shock protein 27 overexpression in transgenic animals against kainate-induced seizures and hippocampal cell death. J Biol Chem 278: 19956-19965, 2003.
33. Straume O, Shimamura T, Lampa MJ, CarreteroJ, Øyan AM, Jia D, Borgman CL and Soucheray M: Suppression of heat shock protein 27 induces long-term dormancy in human breast cancer. Proc Natl Acad Sci USA 109: 8699-8704, 2012.
34. Bauer K, Nitsche U, Slotta-Huspenina J and Drecoll E, Von Weyhern CH, Rosenberg R, Höfler H and Langer R: High HSP27 and HSP70 expression levels are independent adverse prognostic factors in primary resected colon cancer. Cell Oncol (Dordr) 35: 197-205, 2012.
35. Chen SF, Nieh S, Jao SW, Liu CL, Wu CH, Chang YC, Yang CY and Lin YS: Quercetin suppresses drug-resistant spheres via the p38 MAPK-Hsp27 apoptotic pathway in oral cancer cells. PLoS One 7: e49275, 2012.
36. Ciocca DR, Arrigo AP and Calderwood SK: Heat shock proteins and heat shock factor 1 in carcinogenesis and tumor development: an update. Arch Toxicol 87: 19-48, 2013.
37. Pavan S, Musiani D, Torchiaro E, Migliardi G, Gai M, Di Cunto F, Erriquez J, Olivero M and Di Renzo MF: HSP27 is required for invasion and metastasis triggered by hepatocyte growth factor. Int J Cancer 134: 1289-1299, 2013.
38. Acunzo J, Katsogiannou M and Rocchi P: Small heat shock proteins HSP27 (HspB1), αB-crystallin (HspB5) and HSP22 (HspB8) as regulators of cell death. Int J Biochem Cell Biol 44: 1622-1631, 2012.
39. Schmitt E, Gehrmann M, Brunet M, Multhoff G and Garrido C: Intracellular and extracellular functions of heat shock proteins: repercussions in cancer therapy. J Leukoc Biol 81: 15-27, 2007.
40. Voss OH, Batra S, Kolattukudy SJ, Gonzalez-Mejia ME, Smith JB and Doseff AI: Binding of caspase-3 prodomain to heat shock protein 27 regulates monocyte apoptosis by inhibiting caspase-3 proteolytic activation. J Biol Chem 282: 25088-25099, 2007.
41. Rocchi P, Jugpal P, So A, Sinneman S, Ettinger S, Fazli L, Nelson C and Gleave M: Small interference RNA targeting heat-shock protein 27 inhibits the growth of prostatic cell lines and induces apoptosis via caspase-3 activation in vitro. BJU Int 98: 1082-1089, 2006.
42. Paul C, Manero F, Gonin S, Kretz-Remy C, Virot S and Arrigo AP: Hsp27 as a negative regulator of cytochrome c release. Mol Cell Biol 22: 816-834, 2002.
43. Chauhan D, Li G, Hideshima T, Podar K, Mitsiades C, Mitsiades N, Catley L, Tai YT, Hayashi T, Shringarpure R, Burger R, Munshi N, Ohtake Y, Saxena S and Anderson KC: Hsp27 inhibits release of mitochondrial protein Smac in multiple myeloma cells and confers dexamethasone resistance. Blood 102: 3379-3386, 2003.
44. Havasi A, Li Z, Wang Z, Martin JL, Botla V and Ruchalski K: Hsp27 inhibits Bax activation and apoptosis via a phosphatidylinositol 3-kinase-dependent mechanism. J Biol Chem 283: 12305-12313, 2008.
45. Arrigo AP, Virot S, Chaufour S, Firdaus W, Kretz-Remy C and Diaz-Latoud C: Hsp27 consolidates intracellular redox homeostasis by upholding glutathione in its reduced form and by decreasing iron intracellular levels. Antioxid Redox Signal 7: 414-422, 2005.
46. Rogalla T, Ehrnsperger M, Preville X, Kotlyarov A, Lutsch G, Ducasse C, Paul C, Wieske M, Arrigo AP, Buchner J and Gaestel M: Regulation of Hsp27 oligomerization, chaperone function, and protective activity against oxidative stress/tumor necrosis factor alpha by phosphorylation. J Biol Chem 274: 18947-18956, 1999.
47. Sanchez-Niño MD, Sanz AB, Sanchez-Lopez E, Ruiz-Ortega M, Benito-Martin A, Saleem MA, Mathieson PW, Mezzano S, Egido J and Ortiz A: HSP27/HSPB1 as an adaptive podocyte antiapoptotic protein activated by highglucose and angiotensin II. Lab Invest 92: 32-45, 2012.
48. Solary E, Droin N, Bettaieb A, Corcos L, Dimanche-Boitrel MT and Garrido C: Positive and negative regulation of apoptotic pathways by cytotoxic agents in hematological malignancies. Leukemia 14: 1833-1849, 2000.
49. Kamada M, So A, Muramaki M, Rocchi P, Beraldi E and Gleave M: Hsp27 knockdown using nucleotide-based therapies inhibit tumor growth and enhance chemotherapy in human bladder cancer cells. Mol Cancer Ther 6: 299-308, 2007.
50. Heinrich JC, Tuukkanen A, Schroeder M, Fahrig T and Fahrig R: RP101 (brivudine) binds to heat shock protein HSP27 (HSPB1) and enhances survival in animals and pancreatic cancer patients. J Cancer Res Clin Oncol 137: 1349-1361, 2011.
51. Seigneuric R, Gobbo J, Colas P and Garrido C: Targeting cancer with peptide aptamers. Oncotarget 2: 557-561, 2011.
52. Gibert B, Hadchity E, Czekalla A, Aloy MT, Colas P, Rodriguez-Lafrasse C, Arrigo AP and Diaz-Latoud C: Inhibition of heat shock protein 27 (HspB1) tumorigenic functions by peptide aptamers. Oncogene 30: 3672-81, 2011.
53. Kampinga HH, Hageman J, Vos MJ, Kubota H, Tanguay RM, Bruford EA, Cheetham ME, Chen B and Hightower LE: Hightower, Guidelines for the nomenclature of the human heat shock proteins. Cell Stress Chaperones 14: 105-111, 2009.
54. Jäättelä M: Heat shock proteins as cellular lifeguards. Ann Med 31: 261-271, 1999.
55. Beckmann RP, Mizzen LE and Welch WJ: Interaction of Hsp 70 with newly synthesized proteins: Implications for protein folding and assembly. Science 248: 850-854, 1990.
56. Murakami H, Pain D and Blobel G: 70-kD heat shock-related protein is one of at least two distinct cytosolic factors stimulating protein import into mitochondria. J Cell Biol 107: 2051-2057, 1988.
57. Shi Y and Thomas JO: The transport of proteins into the nucleus requires the 70-kilodalton heat shock protein or its cytosolic cognate. Mol Cell Biol 12: 2186-2192, 1992.
58. Nollen EA, Brunsting JF, Roelofsen H, Weber LA and Kampinga HH: In vivo chaperone activity of heat shock protein 70 and thermotolerance. Mol Cell Biol 19: 2069-2079, 1999.
59. Vogel M, Bukau B and Mayer MP: Allosteric regulation of Hsp70 chaperones by a proline switch. Mol Cell 21: 359-367, 2006.
60. Goloudina AR, Demidov ON and Garrido C: Inhibition of HSP70: a challenging anti-cancer strategy. Cancer Lett 325: 117-124, 2012.
61. Bukau B, Weissman J and Horwich A: Molecular chaperones and protein quality control. Cell 125: 443-451, 2006.
62. Schmitt E, Parcellier A, Gurbuxani S, Cande C, Hammann A, Morales MC, Hunt CR, Dix DJ, Kroemer RT, Giordanetto F, Jäättelä M, Penninger JM, Pance A, Kroemer G and Garrido C: Chemosensitization by a non-apoptogenic heat-shock protein 70-binding apoptosis-inducing factor mutant. Cancer Res 63: 8233-8240, 2003.
63. Dix DJ, Allen JW, Collins BW, Mori C, Nakamura N, Poorman-Allen P, Goulding EH and Eddy EM: Targeted gene disruption of Hsp70-2 results in failed meiosis, germ cell apoptosis, and male infertility. Proc Natl Acad Sci USA 93: 3264-3268, 1996.
64. Johnson TR, Stone K and Nikrad M: The proteasome inhibitor PS-341 overcomes TRAIL resistance in Bax and caspase 9-negative or Bcl-xL overexpressing cells. Oncogene 22: 4953-4963, 2003.
65. Hui-qing X, Jian-da Z, Xin-min N, Yan-zhong Z, Cheng-qun L, Quan-yong H, Yi X, Pokharel PB, Shao-hua W and Dan X: HSP70 inhibits burn serum-inducedapoptosis of cardiomyocytes via mitochondrial and membrane death receptor pathways. J Burn Care Res 29: 512-518, 2008.
66. Park HS, Cho SG, Kim CK, Hwang HS, Noh KT, Kim MS, Huh SH, Kim MJ, Ryoo K, Kim EK, Kang WJ, Lee JS, Seo JS, Ko YG, Kim S and Choi EJ: Heat shock protein hsp72 is a negative regulator of apoptosis signal-regulating kinase 1. Mol Cell Biol 22: 7721-7730, 2002.
67. Park HS, Lee JS, Huh SH, Seo JS and Choi EJ: Hsp72 functions as a natural inhibitory protein of c-Jun N-terminal kinase. EMBO J 20: 446-456, 2001.
68. Lee JS, Lee JJ and Seo JS: HSP70 deficiency results in activation of c-Jun N-terminal kinase, extracellular signal-regulated kinase, and caspase-3 in hyperosmolarity-induced apoptosis. J Biol Chem 280: 6634-6641, 2005.
69. Gao T and Newton AC: The turn motif is a phosphorylation switch that regulates the binding of Hsp70 to protein kinase C. J Biol Chem 277: 31585-31592, 2002.
70. Zylicz M, King FW and Wawrzynow A: Hsp70 interactions with the p53 tumour suppressor protein. EMBO J 20: 4634-4638, 2001.
71. Yang X, Wang J, Zhou Y, Wang Y, Wang S and Zhang W: Hsp70 promotes chemoresistance by blocking Bax mitochondrial translocation in ovariancancer cells. Cancer Lett 321: 137-143, 2012.
72. Stankiewicz AR, Lachapelle G, Foo CP, Radicioni SM and Mosser DD: Hsp70 inhibits heat-induced apoptosis upstream of mitochondria by preventing Bax translocation. J Biol Chem 280: 38729-38739, 2005.
73. Li CY, Lee JS, Ko YG, Kim JI and Seo JS: Heat shock protein 70 inhibits apoptosis down-stream of cytochrome c release and upstream of caspase-3 activation. J Biol Chem 275: 25665-25671, 2000.
74. Beere HM, Wolf BB, Cain K, Mosser DD, Mahboubi A, Kuwana T, Tailor P, Morimoto RI, Cohen GM and Green DR: Heat-shock protein 70 inhibits apoptosis by preventing recruitment of procaspase-9 to the Apaf-1 apoptosome. Nat Cell Biol 2: 469-475, 2000.
75. Creagh EM, Carmody RJ and Cotter TG: Heat shock protein 70 inhibits caspase-dependent and-independent apoptosis in Jurkat T cells. Exp Cell Res 257: 58-66, 2000.
76. Ravagnan L, Gurbuxani S, Susin SA, Maisse C, Daugas E, Zamzami N, Mak T, Jaattela M, Penninger JM, Garrido C and Kroemer G: Heat-shock protein 70 antagonizes apoptosis-inducing factor. Nat Cell Biol 3: 839-843, 2001.
77. Gurbuxani S, Schmitt E, Cande C, Parcellier A, Hammann A, Daugas E, Kouranti I, Spahr C, Pance A, Kroemer G and Garrido C: Heat shock protein 70 binding inhibits the nuclear import of apoptosis-inducing factor. Oncogene 22: 6669-6678, 2003.
78. Matsumori Y, Hong SM, Aoyama K, Fan Y, Kayama T, Sheldon RA, Vexler ZS, Ferriero DM, Weinstein PR and Liu J: Hsp70 overexpression sequesters AIF and reduces neonatal hypoxic/ischemic brain injury. J Cereb Blood Flow Metab 25: 899-910, 2005.
79. Kalinowska M, Garncarz W, Pietrowska M, Garrard WT and Widlak P: Regulation of the human apoptotic DNase/RNase endonuclease G: Involvement of Hsp70 and ATP. Apoptosis 10: 821-830, 2005.
80. Sakahira H and Nagata S: Cotranslational folding of caspase-activated DNase with Hsp70, Hsp40, and inhibitor of caspase-activated DNase. J Biol Chem 277: 3364-3370, 2002.
81. Liu QL, Kishi H, Ohtsuka K and Muraguchi A: Heat shock protein 70 binds caspase-activated DNase and enhances its activity in TCR-stimulated T cells. Blood 102: 1788-1796, 2003.
82. Ribeil JA, Zermati Y, Vandekerckhove J, Cathelin S, Kersual J, Dussiot M, Coulon S, Moura IC, Zeuner A, Kirkegaard-Sørensen T, Varet B, Solary E, Garrido C and Hermine O: Hsp70 regulates erythropoiesis by preventing caspase-3-mediated cleavage of GATA-1. Nature 445: 102-105, 2007.
83. Gyrd-Hansen M, Nylandsted J and Jaattela M: Heat shock protein 70 promotes cancer cell viability by safeguarding lysosomal integrity. Cell Cycle 3: 1484-1485, 2004.
84. Nylandsted J, Gyrd-Hansen M, Danielewicz A, Fehrenbacher N, Lademann U, Hoyer-Hansen M,Weber E, Multhoff G, Rohde M and Jaattela M: Heat shock protein 70 promotes cell survival by inhibiting lysosomal membrane permeabilization. J Exp Med 200: 425-435, 2004.
85. Leu JI, Pimkina J, Frank A, Murphy ME and George DL: A small molecule inhibitor of inducible heat shock protein 70. Mol Cell 36: 15-27, 2009.
86. Schmitt E, Maingret L, Puig PE, Rerole AL, Ghiringhelli F, Hammann A, Solary E, Kroemer G and Garrido C: Heat-shock protein 70 neutralization exerts potent antitumor effects in animal models of colon cancer and melanoma. Cancer Res 66: 4191-4197, 2006.
87. Nadeau K, Nadler SG, Saulnier M, Tepper MA and Walsh CT: Quantitation of the interaction of the immunosuppressant deoxyspergualin and analogs with Hsc70 and Hsp90. Biochemistry 33: 2561-2567, 1994.
88. Fewell SW, Day BW and Brodsky JL: Identification of an inhibitor of hsc70-mediated protein translocation and ATP hydrolysis. J Biol Chem 276: 910-914, 2001.
89. Rodina A, Vilenchik M, Moulick K, Aguirre J, Kim J, Chiang A, Litz J, Clement CC, Kang Y, She Y, Wu N, Felts S, Wipf P, Massague J, Jiang X, Brodsky JL, Krystal GW and Chiosis G: Selective compounds define Hsp90 as a major inhibitor of apoptosis in small-cell lung cancer. Nat Chem Biol 3: 498-507, 2007.
90. Wright CM, Seguin SP, Fewell SW, Zhang H, Ishwad C, Vats A, Lingwood CA, Wipf P, Fanning E, Pipas JM and Brodsky JL: Inhibition of SimianVirus 40 replication by targeting the molecular chaperone function and ATPase activity of T antigen. Virus Res 141: 71-80, 2009.
91. Massey AJ, Williamson DS, Browne H, Murray JB, Dokurno P, Shaw T, Macias AT, Daniels Z, Geoffroy S, Dopson M, Lavan P, Matassova N, Francis GL, Graham CJ, Parsons R, Wang Y, Padfield A, Comer M, Drysdale MJ and Wood M: A novel, small molecule inhibitor of Hsc70/Hsp70 potentiates Hsp90 inhibitor induced apoptosis in HCT116 colon carcinoma cells. Cancer Chemother Pharmacol 66: 535-545, 2010.
92. Jinwal UK, Miyata Y, Koren J III, Jones JR, Trotter JH, Chang L, O'Leary J, Morgan D, Lee DC, Shults CL, Rousaki A, Weeber EJ, Zuiderweg ER, Gestwicki JE and Dickey CA: Chemical manipulation of hsp70 ATPase activity regulates tau stability. J Neurosci 29: 12079-88, 2009.
93. Wadhwa R, Sugihara T, Yoshida A, Nomura H, Reddel RR, Simpson R, Maruta H and Kaul SC: Selective toxicity of MKT-077 to cancer cells is mediated by its binding to the hsp70 family protein mot-2 and reactivation of p53 function. Cancer Res 60: 6818-6821, 2000.
94. Wadhwa R, Yaguchi T, Hasan MK, Mitsui Y, Reddel RR and Kaul SC: Hsp70 family member, mot-2/mthsp70/GRP75, binds to the cytoplasmic sequestration domain of the p53 protein. Exp Cell Res 274: 246-253, 2002.
95. Britten CD, Rowinsky EK, Baker SD, Weiss GR, Smith L, Stephenson J, Rothenberg M,Smetzer L, Cramer J, Collins W, Von Hoff DD and Eckhardt SG: A phase I and pharmacokinetic study of the mitochondrial-specific rhodacyanine dye analog MKT 077. Clin Cancer Res 6: 42-49, 2000.
96. Williams DR, Ko SK, Park S, Lee MR and Shin I: An apoptosis-inducing small molecule that binds to heat shock protein 70. Angew Chem Int Ed Engl 47: 7466-7469, 2008.
97. Powers MV, Jones K, Barillari C, Westwood I, van Montfort RL and Workman P: Targeting HSP70: the second potentially druggable heat shock protein and molecular chaperone? Cell Cycle 9: 1542-1550, 2010.
98. Whetstone H and Lingwood C: 3′Sulfogalactolipid binding specifically inhibits Hsp70 ATPase activity in vitro. Biochemistry 42: 1611-1617, 2003.
99. Chatterjee M, Andrulis M, Stühmer T, Müller E, Hofmann C, Steinbrunn T, Heimberger T, Schraud H, Kressmann S, Einsele H and Bargou RC: The PI3K/Akt signaling pathway regulates the expression of Hsp70, which critically contributes to Hsp90-chaperone function and tumor cell survival in multiple myeloma. Haematologica 98: 1132-1141, 2013.
100. Multhoff G and Radons J: Radiation, inflammation, and immune responses in cancer. Front Oncol 2: 58, 2012.
101. Stangl S, Gehrmann M, Riegger J, Kuhs K, Riederer I, Sievert W, Hube K, Mocikat R, Dressel R, Kremmer E, Pockley AG, Friedrich L, Vigh L, Skerra A and Multhoff G: Targeting membrane heat-shock protein 70 (Hsp70) on tumors by cmHsp70.1 antibody. Proc Nat Acad Sci USA 108: 733-738, 2011.
102. Krause SW, Gastpar R, Andreesen R, Gross C, Ullrich H, Thonigs G, Pfister K and Multhoff G: Treatment of colon and lung cancer patients with ex vivo heat shock protein 70-peptide-activated, autologous natural killer cells: a clinical phase I trial. Clin Cancer Res 10: 3699-3707, 2004.
103. Whitesell L and Lindquist SL: HSP90 and the chaperoning of cancer. Nat Rev Cancer 5: 761-772, 2005.
104. Taipale M, Jarosz DF and Lindquist S: HSP90 at the hub of protein homeostasis: emerging mechanistic insights. Nat Rev Mol Cell Biol 11: 515-528, 2010.
105. Sreedhar AS, Kalmár E, Csermely P and Shen YF: Hsp90 isoforms: functions, expression and clinical importance. FEBS Lett 562: 11-15, 2004.
106. Hartl FU, Bracher A and Hayer-Hartl M: Molecular chaperones in protein folding and proteostasis. Nature 475: 324-332, 2011.
107. Onuoha SC, Coulstock ET, Grossmann JG and Jackson SE: Structural studies on the co-chaperone Hop and its complexes with Hsp90. J Mol Biol 379: 732-744, 2008.
108. Mayer MP: Gymnastics of molecular chaperones. Mol Cell 39: 321-331, 2010.
109. Krukenberg KA, Street TO, Lavery LA and Agard DA: Conformational dynamics of the molecular chaperone Hsp90. Q Rev Biophys 44: 229-255, 2011.
110. Ali MM, Roe SM, Vaughan CK, Meyer P, Panaretou B and Piper PW: Crysta l structure of an Hsp90-nucleotide-p23/Sba1 closed chaperone complex. Nature 440: 1013-1017, 2006.
111. Normant E, Paez G and West KA: The Hsp90 inhibitor IPI-504 rapidly lowers EML4-ALK levels and induces tumor regression in ALK-driven NSCLC models. Oncogene 30: 2581-2586, 2011.
112. Neckers L and Workman P: HSP90 molecular chaperone inhibitors: are we there yet? Clin Cancer Res 18: 64-76, 2012.
113. Modi S, Stopeck A and Linden H: HSP90 inhibition is effective in breast cancer: a phase II trial of tanespimycin (17-AAG) plus trastuzumab in patients with HER2-positive metastatic breast cancer progressing on trastuzumab. Clin Cancer Res 17: 5132-5139, 2011.
114. Hanahan D and Weinberg RA: Hallmarks of cancer: the next generation. Cell 144: 646-674, 2011.
115. Khong T and Spencer A: Targeting HSP 90 induces apoptosis and inhibits critical survival and proliferation pathways in multiple myeloma. Mol Cancer Ther 10: 1909-1917, 2011.
116. Workman P, Burrows F, Neckers L and Rosen N: Drugging the cancer chaperone HSP90: combinatorial therapeutic exploitation of oncogene addiction and tumor stress. Ann NY Acad Sci 1113: 202-216, 2007.
117. Hartl FU: Chaperone-assisted protein folding: the path to discovery from a personal perspective. Nat Med 17: 1206-1210, 2011.
118. Tiroli-Cepeda AO and Ramos CH: An overview of the role of molecular chaperones in protein homeostasis. Protein Pept Lett 18: 101-109, 2011.
119. Patel HJ, Modi S, Chiosis G and Taldone T: Advances in the discovery and development of heat-shock protein 90 inhibitors for cancer treatment. Expert Opin Drug Discov 6: 559-587, 2011.
120. Sequist LV, Gettinger S and Natale R: A phase II trial of IPI-504 (retaspimycin hydrochloride), a novel Hsp90 inhibitor, in patients with relapsed and/or refractory stage IIIb or stage IV non-small cell lung cancer (NSCLC) stratified by EGFR mutation status. J Clin Oncol 27: 15s, 2009.
121. McCollum AK, Teneyck CJ, Sauer BM, Toft DO and Erlichman C: Up-regulation of heat shock protein 27 induces resistance to 17-allylamino-demethoxy geldanamycin through a glutathione-mediated mechanism. Cancer Res 66: 10967-10975, 2006.
122. Didelot C, Lanneau D, Brunet M, Bouchot A, Cartier J, Jacquel A, Ducoroy P, Cathelin S, Decologne N, Chiosis G, Dubrez-Daloz L, Solary E and Garrido C: Interaction of heat-shock protein 90 beta isoform (HSP90 beta) with cellular inhibitor of apoptosis 1 (c-IAP1) is required for cell differentiation. Cell Death Differ 15: 859-866, 2008.
123. Eustace BK, Sakurai T, Stewart JK, Yimlamai D, Unger C, Zehetmeier C, Lain B, Torella C, Henning SW, Beste G, Scroggins BT, Neckers L, Ilag LL and Jay DG: Functional proteomic screens reveal an essential extracellular role for hsp90 alpha in cancer cell invasiveness. Nat Cell Biol 6: 507-514, 2004.
124. Wang X, Song X, Zhuo W, Fu Y, Shi H, Liang Y, Tong M, Chang G and Luo Y: The regulatory mechanism of Hsp90 alpha secretion and its function in tumor malignancy. Proc Natl Acad Sci USA 106: 21288-21293, 2009.